Skip to main content
SpringerLink
Log in

The coronafacoyl phytotoxins: structure, biosynthesis, regulation and biological activities

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Phytotoxins are secondary metabolites that contribute to the development and/or severity of diseases caused by various plant pathogenic microorganisms. The coronafacoyl phytotoxins are an important family of plant toxins that are known or suspected to be produced by several phylogenetically distinct plant pathogenic bacteria, including the gammaproteobacterium Pseudomonas syringae and the actinobacterium Streptomyces scabies. At least seven different family members have been identified, of which coronatine was the first to be described and is the best-characterized. Though nonessential for disease development, coronafacoyl phytotoxins appear to enhance the severity of disease symptoms induced by pathogenic microbes during host infection. In addition, the identification of coronafacoyl phytotoxin biosynthetic genes in organisms not known to be plant pathogens suggests that these metabolites may have additional roles other than as virulence factors. This review focuses on our current understanding of the structures, biosynthesis, regulation, biological activities and evolution of coronafacoyl phytotoxins as well as the different methods that are used to detect these metabolites and the organisms that produce them.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anton N, Santos-Aberturas J, Mendes MV, Guerra SM, Martin JF, Aparicio JF (2007) PimM, a PAS domain positive regulator of pimaricin biosynthesis in Streptomyces natalensis. Microbiology 153:3174–3183

    Article  CAS  PubMed  Google Scholar 

  • Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, Cherkis K, Roach J, Grant SR, Jones CD, Dangl JL (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7:e1002132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clement C, Ouhdouch Y, Van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43

    Article  PubMed  Google Scholar 

  • Bell KS, Sebaihia M, Pritchard L, Holden MT, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJ, Mungall K, Atkin R, Bason N, Brooks K, Chillingworth T, Clark K, Doggett J, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Norbertczak H, Ormond D, Price C, Quail MA, Sanders M, Walker D, Whitehead S, Salmond GP, Birch PR, Parkhill J, Toth IK (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101:11105–11110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender CL (1999) Chlorosis-inducing phytotoxins produced by Pseudomonas syringae. Eur J Plant Pathol 105:1–12

    Article  CAS  Google Scholar 

  • Bender CL, Alarcon-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63:266–292

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bent AF, Innes RW, Ecker JR, Staskawicz BJ (1992) Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant-Microbe Interact 5:372–378

    Article  CAS  PubMed  Google Scholar 

  • Bignell DRD, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry R, Loria R (2010) Streptomyces scabies 87-22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant-microbe interactions. Mol Plant-Microbe Interact 23:161–175

    Article  CAS  PubMed  Google Scholar 

  • Bignell DRD, Francis IM, Fyans JK, Loria R (2014) Thaxtomin A production and virulence are controlled by several bld gene global regulators in Streptomyces scabies. Mol Plant-Microbe Interact 27:875–885

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Joardar V, Gao L, Robertson TL, Lim M, Kunkel BN (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44:73–88

    Article  CAS  PubMed  Google Scholar 

  • Bown L, Altowairish MS, Fyans JK, Bignell DRD (2016) Production of the Streptomyces scabies coronafacoyl phytotoxins involves a novel biosynthetic pathway with an F420-dependent oxidoreductase and a short-chain dehydrogenase/reductase. Mol Microbiol 101:122–135

    Article  CAS  PubMed  Google Scholar 

  • Bown L, Li Y, Berrue F, Verhoeven JTP, Dufour SC, Bignell DRD (2017) Coronafacoyl phytotoxin biosynthesis and evolution in the common scab pathogen Streptomyces scabies. Appl Environ Microbiol 83:e01169

    Article  CAS  PubMed Central  Google Scholar 

  • Brady CL, Cleenwerck I, Denman S, Venter SN, Rodriguez-Palenzuela P, Coutinho TA, De Vos P (2012) Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov. and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int J Syst Evol Microbiol 62:1592–1602

    Article  CAS  PubMed  Google Scholar 

  • Braun Y, Smirnova AV, Weingart H, Schenk A, Ullrich MS (2007) A temperature-sensing histidine kinase: function, genetics, and membrane topology. Methods Enzymol 423:222–249

    Article  CAS  PubMed  Google Scholar 

  • Budde IP, Rohde BH, Bender CL, Ullrich MS (1998) Growth phase and temperature influence promoter activity, transcript abundance, and protein stability during biosynthesis of the Pseudomonas syringae phytotoxin coronatine. J Bacteriol 180:1360–1367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bull CT, Manceau C, Lydon J, Kong H, Vinatzer BA, Fischer-Le Saux M (2010) Pseudomonas cannabina pv. cannabina pv. nov., and Pseudomonas cannabina pv. alisalensis (Cintas Koike and Bull, 2000) comb. nov., are members of the emended species Pseudomonas cannabina (ex Sutic & Dowson 1959) Gardan, Shafik, Belouin, Brosch, Grimont and Grimont 1999. Syst Appl Microbiol 33:105–115

    Article  PubMed  Google Scholar 

  • Chan YA, Podevels AM, Kevany BM, Thomas MG (2009) Biosynthesis of polyketide synthase extender units. Nat Prod Rep 26:90–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chater KF (2006) Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Philos Trans R Soc Lond B 361:761–768

    Article  CAS  Google Scholar 

  • Cheng Z, Bown L, Tahlan K, Bignell DRD (2015) Regulation of coronafacoyl phytotoxin production by the PAS-LuxR family regulator CfaR in the common scab pathogen Streptomyces scabies. PLoS ONE 10:e0122450

    Article  PubMed  PubMed Central  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Cintas NA, Koike ST, Bull CT (2002) A new pathovar, Pseudomonas syringae pv. alisalensis pv. nov., proposed for teh causal agent of bacterial blight of broccoli and broccoli raab. Plant Dis 86:992–998

    Article  Google Scholar 

  • Couch R, O’connor SE, Seidle H, Walsh CT, Parry R (2004) Characterization of CmaA, an adenylation-thiolation didomain enzyme involved in the biosynthesis of coronatine. J Bacteriol 186:35–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson IB, Mitchell RE (1985) Stimulation of ethylene production in bean leaf discs by the pseudomonad phytotoxin coronatine. Plant Physiol 77:969–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  CAS  PubMed  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fyans JK, Altowairish MS, Li Y, Bignell DRD (2015) Characterization of the coronatine-like phytotoxins produced by the common scab pathogen Streptomyces scabies. Mol Plant-Microbe Interact 28:443–454

    Article  CAS  PubMed  Google Scholar 

  • Gardan L, Shafik H, Belouin S, Broch R, Grimont F, Grimont PA (1999) DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int J Syst Bacteriol 49(2):469–478

    Article  CAS  PubMed  Google Scholar 

  • Gardan L, Gouy C, Christen R, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Microbiol 53:381–391

    Article  CAS  PubMed  Google Scholar 

  • Geng X, Cheng J, Gangadharan A, Mackey D (2012) The coronatine toxin of Pseudomonas syringae is a multifunctional suppressor of Arabidopsis defense. Plant Cell 24:4763–4774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gnanamanickam SS, Starratt AN, Ward EWB (1982) Coronatine production in vitro and in vivo and its relation to symptom development in bacterial blight of soybean. Can J Bot 60:645–650

    Article  CAS  Google Scholar 

  • Gross H, Loper JE (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

    Article  CAS  PubMed  Google Scholar 

  • Han HS, Koh YJ, Hur JS, Jung JS (2003) Identification and charcterization of coronatine-producing Pseudomonas syringae pv actinidiae. J Microbiol Biotechnol 13:110–118

    CAS  Google Scholar 

  • Hauser E, Kampfer P, Busse HJ (2004) Pseudomonas psychrotolerans sp. nov. Int J Syst Evol Microbiol 54:1633–1637

    Article  CAS  PubMed  Google Scholar 

  • Ichihara A, Toshima H (1999) Coronatine: chemistry and biological activities. In: Cutler HG and Cutler SJ (eds) Biologically active natural products: agrochemicals. CRC Press

  • Ichihara A, Shiraishi K, Sato H, Sakamura S, Nishiyama K, Sakai R, Furusaki A, Matsumoto T (1977) The structure of coronatine. J Am Chem Soc 99:636–637

    Article  CAS  Google Scholar 

  • Jeong H, Kloepper JW, Ryu CM (2015) Genome sequences of Pseudomonas amygdali pv. tabaci strain ATCC 11528 and pv. lachrymans strain 98A-744. Genome Announc 3(3):e00683

  • Jones WT, Harvey D, Mitchell RE, Ryan GB, Bender CL, Reynolds PH (1997) Competitive ELISA employing monoclonal antibodies specific for coronafacoyl amino acid conjugates. Food Agric Immunol 9:67–76

    Article  CAS  Google Scholar 

  • Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H, Kawaharada Y, Nakamura Y, Watanabe A, Kawashima K, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Sato S (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly WL, Boyne MT 2nd, Yeh E, Vosburg DA, Galonic DP, Kelleher NL, Walsh CT (2007) Characterization of the aminocarboxycyclopropane-forming enzyme CmaC. Biochemistry 46:359–368

    Article  CAS  PubMed  Google Scholar 

  • Kenyon JS, Turner JG (1992) The stimulation of ethylene synthesis in Nicotiana tabacum leaves by the phytotoxin coronatine. Plant Physiol 100:219–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XZ, Starratt AN, Cuppels DA (1998) Identification of tomato leaf factors that activate toxin gene expression in Pseudomonas syringae pv. tomato DC3000. Phytopathology 88:1094–1100

    Article  CAS  PubMed  Google Scholar 

  • Liyanage H, Palmer DA, Ullrich M, Bender CL (1995) Characterization and transcriptional analysis of the gene cluster for coronafacic acid, the polyketide component of the phytotoxin coronatine. Appl Environ Microbiol 61:3843–3848

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma S-W, Morris VL, Cuppels DA (1991) Characterization of a DNA region required for production of the phytotoxin coronatine by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 4:69–74

    Article  CAS  Google Scholar 

  • Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY (2008a) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melotto M, Underwood W, He SY (2008b) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Midha S, Bansal K, Sharma S, Kumar N, Patil PP, Chaudry V, Patil PB (2016) Genomic resource of rice seed associated bacteria. Front Microbiol 6:1551

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell RE (1984) A naturally-ocurring structural analogue of the phytotoxin coronatine. Phytochemistry 23:791–793

    Article  CAS  Google Scholar 

  • Mitchell RE (1991) Implications of toxins in the ecology and evolution of plant pathogenic microorganisms bacteria. Experientia 47:791–803

    Article  CAS  PubMed  Google Scholar 

  • Mitchell RE, Young H (1985) N-coronafacoyl-l-isoleucine and N-coronafacoyl-l-alloisoleucine, potential biosynthetic intermediates of the phytotoxin coronatine. Phytochemistry 24:2716–2717

    Article  CAS  Google Scholar 

  • Nishiyama K, Sakai R, Ezuka A, Ichihara A, Shiraishi K, Ogaswara M, Sato H, Sakamura S (1976) Phytotoxic effects of coronatine produced by Pseudomonas coronafaciens var. atropurpurea on leaves of Italian ryegrass. Ann Phytopathol Soc Jpn 42:613–614

    Article  Google Scholar 

  • Okamoto T, Taguchi H, Nakamura K, Ikenaga H, Kuraishi H, Yamasato K (1993) Zymobacter palmae gen. nov., sp. nov., a new ethanol-fermenting peritrichous bacterium isolated from palm sap. Arch Microbiol 160:333–337

    Article  CAS  PubMed  Google Scholar 

  • Palmer DA, Bender CL (1993) Effects of environmental and nutritional factors on production of the polyketide phytotoxin coronatine by Pseudomonas syringae pv. glycinea. Appl Environ Microbiol 59:1619–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer DA, Bender CL (1995) Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Mol Plant Microbe Interact 8:683–692

    Article  CAS  Google Scholar 

  • Panchal S, Breitbach ZS, Melotto M (2017) An HPLC-based method to quantify coronatine produced by bacteria. Bio-Protocol 7:e2147

    Article  PubMed  PubMed Central  Google Scholar 

  • Panda P, Vanga BR, Lu A, Fiers M, Fineran PC, Butler R, Armstrong K, Ronson CW, Pitman AR (2016) Pectobacterium atrosepticum and Pectobacterium carotovorum harbor distinct, independently acquired integrative and conjugative elements encoding coronafacic acid that enhance virulence on potato stems. Front Microbiol 7:397

    Article  PubMed  PubMed Central  Google Scholar 

  • Pao GM, Tam R, Lipschitz LS, Saier MH Jr (1994) Response regulators: structure, function and evolution. Res Microbiol 145:356–362

    Article  CAS  PubMed  Google Scholar 

  • Parry RJ, Mhaskar SV, Lin M-T, Walker AE, Mafoti R (1994) Investigations of the biosynthesis of coronamic acid. Can J Chem 72:86–99

    Article  CAS  Google Scholar 

  • Parry RJ, Jiralerspong S, Mhaskar S, Alemany L, Willcott R (1996) Investigations of coronatine biosynthesis. Elucidation of the mode of incorporation of pyruvate into coronafacic acid. J Am Chem Soc 118:703–704

    Article  CAS  Google Scholar 

  • Patel J, Hoyt JC, Parry RJ (1998) Investigations of coronatine biosynthesis. Overexpression and assay of CmaT, a thioesterase involved in coronamic acid biosynthesis. Tetrahedron 54:15927–15936

    Article  CAS  Google Scholar 

  • Penaloza-Vazquez A, Bender CL (1998) Characterization of CorR, a transcriptional activator which is required for biosynthesis of the phytotoxin coronatine. J Bacteriol 180:6252–6259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Penfold CN, Bender CL, Turner JG (1996) Characterisation of genes involved in biosynthesis of coronafacic acid, the polyketide component of the phytotoxin coronatine. Gene 183:167–173

    Article  CAS  PubMed  Google Scholar 

  • Qi M, Wang D, Bradley CA, Zhao Y (2011) Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine pseudomonads. PLoS ONE 6:e16451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rangaswamy V, Bender CL (2000) Phosphorylation of CorS and CorR, regulatory proteins that modulate production of the phytotoxin coronatine in Pseudomonas syringae. FEMS Microbiol Lett 193:13–18

    Article  CAS  PubMed  Google Scholar 

  • Rangaswamy V, Ullrich M, Jones W, Mitchell R, Parry R, Reynolds P, Bender CL (1997) Expression and analysis of coronafacate ligase, a thermoregulated gene required for production of the phytotoxin coronatine in Pseudomonas syringae. FEMS Microbiol Lett 154:65–72

    Article  CAS  PubMed  Google Scholar 

  • Rangaswamy V, Jiralerspong S, Parry R, Bender CL (1998a) Biosynthesis of the Pseudomonas polyketide coronafacic acid requires monofunctional and multifunctional polyketide synthase proteins. Proc Natl Acad Sci USA 95:15469–15474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rangaswamy V, Mitchell R, Ullrich M, Bender C (1998b) Analysis of genes involved in biosynthesis of coronafacic acid, the polyketide component of the phytotoxin coronatine. J Bacteriol 180:3330–3338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rohde BH, Pohlack B, Ullrich MS (1998) Occurrence of thermoregulation of genes involved in coronatine biosynthesis among various Pseudomonas syringae strains. J Basic Microbiol 38:41–50

    Article  CAS  PubMed  Google Scholar 

  • Sakai R, Nishiyama K, Ichihara A, Shiraishi K, Sakamura S (1979) Studies on the mechanism of physiological activity of coronatine. Effect of coronatine on cell wall extensibility and expansion of potato tuber tissue. Ann Phytopath Soc Jpn 45:645–653

    Article  Google Scholar 

  • Samson R, Legendre JB, Christen R, Fischer-Le Saux M, Achouak W, Gardan L et al (2005) Transfer of Pectobacterium chrysanthemi (Burkholder 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 55:1415–1427

    Article  CAS  PubMed  Google Scholar 

  • Santos-Aberturas J, Vicente CM, Guerra SM, Payero TD, Martin JF, Aparicio JF (2011) Molecular control of polyene macrolide biosynthesis: direct binding of the regulator PimM to eight promoters of pimaricin genes and identification of binding boxes. J Biol Chem 286:9150–9161

    Article  CAS  PubMed  Google Scholar 

  • Sarris PF, Trantas EA, Baltrus DA, Bull CT, Wechter WP, Yan S, Ververidis F, Almeida NF, Jones CD, Dangl JL, Panopoulos NJ, Vinatzer BA, Goumas DE (2013) Comparative genomics of multiple strains of Pseudomonas cannabina pv. alisalensis, a potential model pathogen of both monocots and dicots. PLoS ONE 8:e59366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, O’donnell P, Sammons M, Toshima H, Tumlinson JH 3rd (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Nat Acad Sci USA 100:10552–10557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiraishi K, Konoma K, Sato H, Ichihara A, Sakamura S, Nishiyama K, Sakai R (1979) The structure-activity relationships in coronatine analogs and amino compounds derived from (+)-coronafacic acid. Agric Biol Chem 43:1753–1757

    CAS  Google Scholar 

  • Slawiak M, Lojkowska E (2009) Genes responsible for coronatine synthesis in Pseudomonas syringae present in the genome of soft rot bacteria. Eur J Plant Pathol 124:353–361

    Article  CAS  Google Scholar 

  • Smirnova AV, Ullrich MS (2004) Topological and deletion analysis of CorS, a Pseudomonas syringae sensor kinase. Microbiology 150:2715–2726

    Article  CAS  PubMed  Google Scholar 

  • Sreedharan A, Penaloza-Vazquez A, Kunkel BN, Bender CL (2006) CorR regulates multiple components of virulence in Pseudomonas syringae pv. tomato DC3000. Mol Plant-Microbe Interact 19:768–779

    Article  CAS  PubMed  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    Article  CAS  PubMed  Google Scholar 

  • Strange RN (2007) Phytotoxins produced by microbial plant pathogens. Nat Prod Rep 24:127–144

    Article  CAS  PubMed  Google Scholar 

  • Strieter ER, Vaillancourt FH, Walsh CT (2007) CmaE: a transferase shuttling aminoacyl groups between carrier protein domains in the coronamic acid biosynthetic pathway. Biochemistry 46:7549–7557

    Article  CAS  PubMed  Google Scholar 

  • Strieter ER, Koglin A, Aron ZD, Walsh CT (2009) Cascade reactions during coronafacic acid biosynthesis: elongation, cyclization, and functionalization during Cfa7-catalyzed condensation. J Am Chem Soc 131:2113–2115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundin GW (2007) Genomic insights into the contribution of phytopathogenic bacterial plasmids to the evolutionary history of their hosts. Annu Rev Phytopathol 45:129–151

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Takikawa Y, Tsuyumu S, Goto M, Watanabe M (1992) Coronatine production by Xanthomonas campestris pv. phormiicola. Ann Phytopath Soc Japan 58:276–281

    Article  CAS  Google Scholar 

  • Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Ullrich M, Bender CL (1994) The biosynthetic gene cluster for coronamic acid, an ethylcyclopropyl amino acid, contains genes homologous to amino acid-activating enzymes and thioesterases. J Bacteriol 176:7574–7586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullrich M, Penaloza-Vazquez A, Bailey AM, Bender CL (1995) A modified two-component regulatory system is involved in temperature-dependent biosynthesis of the Pseudomonas syringae phytotoxin coronatine. J Bacteriol 177:6160–6169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uppalapati SR, Ayoubi P, Weng H, Palmer DA, Mitchell RE, Jones W, Bender CL (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42:201–217

    Article  CAS  PubMed  Google Scholar 

  • Vaillancourt FH, Yeh E, Vosburg DA, O’connor SE, Walsh CT (2005) Cryptic chlorination by a non-haem iron enzyme during cyclopropyl amino acid biosynthesis. Nature 436:1191–1194

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela-Soto JH, Maldonado-Bonilla LD, Hernandez-Guzman G, Rincon-Enriquez G, Martinez-Gallardo NA, Ramirez-Chavez E, Hernandez IC, Hernandez-Flores JL, Delano-Frier JP (2015) Infection by a coronatine-producing strain of Pectobacterium cacticidum isolated from sunflower plants in Mexico is characterized by soft rot and chlorosis. J Gen Plant Pathol 81:368–381

    Article  CAS  Google Scholar 

  • Vanga BR, Butler RC, Toth IK, Ronson CW, Pitman AR (2012) Inactivation of PbTopo IIIbeta causes hyper-excision of the pathogenicity island HAI2 resulting in reduced virulence of Pectobacterium atrosepticum. Mol Microbiol 84:648–663

    Article  CAS  PubMed  Google Scholar 

  • Vanga BR, Ramakrishnan P, Butler RC, Toth IK, Ronson CW, Jacobs JM, Pitman AR (2015) Mobilization of horizontally acquired island 2 is induced in planta in the phytopathogen Pectobacterium atrosepticum SCRI1043 and involves the putative relaxase ECA0613 and quorum sensing. Environ Microbiol 17:4730–4744

    Article  CAS  PubMed  Google Scholar 

  • Volksch B, Bublitz F, Fritsche W (1989) Coronatine production by Pseudomonas syringae pathovars: screening method and capacity of product formation. J Basic Microbiol 29:463–468

    Article  Google Scholar 

  • Wang L, Bender CL, Ullrich MS (1999) The transcriptional activator CorR is involved in biosynthesis of the phytotoxin coronatine and binds to the cmaABT promoter region in a temperature-dependent manner. Mol Gen Genet 262:250–260

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weingart H, Stubner S, Schenk A, Ullrich MS (2004) Impact of temperature on in planta expression of genes involved in synthesis of the Pseudomonas syringae phytotoxin coronatine. Mol Plant Microbe Interact 17:1095–1102

    Article  CAS  PubMed  Google Scholar 

  • Wilson MC, Moore BS (2012) Beyond ethylmalonyl-CoA: the functional role of crotonyl-CoA carboxylase/reductase homologs in expanding polyketide diversity. Nat Prod Rep 29:72–86

    Article  CAS  PubMed  Google Scholar 

  • Worley JN, Russell AB, Wexler AG, Bronstein PA, Kvitko BH, Krasnoff SB, Munkvold KR, Swingle B, Gibson DM, Collmer A (2013) Pseudomonas syringae pv. tomato DC3000 CmaL (PSPTO4723), a DUF1330 family member, is needed to produce l-allo-isoleucine, a precursor for the phytotoxin coronatine. J Bacteriol 195:287–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xin XF, He SY (2013) Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 51:473–498

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

D.R.D. Bignell acknowledges support from the Natural Science and Engineering Research Council of Canada Discovery Grants program (Grant no. 386696-2010), the Canada Foundation for Innovation Leaders Opportunity Fund (Project no. 30482) and the Newfoundland and Labrador Research and Development Corporation Leverage R&D program (Project No. 5404.1218.103).

Author information

Author notes

  1. Authors Zhenlong Cheng and Luke Bown contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Memorial University of Newfoundland, St. John’s, NL, A1B 3X9, Canada

    Dawn R. D. Bignell, Zhenlong Cheng & Luke Bown

Authors
  1. Dawn R. D. Bignell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenlong Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luke Bown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dawn R. D. Bignell.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (PDF 122 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bignell, D.R.D., Cheng, Z. & Bown, L. The coronafacoyl phytotoxins: structure, biosynthesis, regulation and biological activities. Antonie van Leeuwenhoek 111, 649–666 (2018). https://doi.org/10.1007/s10482-017-1009-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-017-1009-1

Keywords

Search

Navigation